Histamine: A Neurotransmitter Candidate for <i>Drosophila</i> Photoreceptors

Sarthy, P. Vijay

doi:10.1111/j.1471-4159.1991.tb06378.x

Cited by 90 publications

(84 citation statements)

References 59 publications

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“…In visual tissues of the horseshoe crab Limulus polyphemus, most histamine is metabolized to imidazole acetic acid and γ-glutamyl histamine (23). Although N-acetylation of histamine in arthropods has not been studied, N-acetyl histamine has been detected in locusts and Drosophila (24,25), suggesting that arthropods might have a histamine NAT. The identification of histamine acetylation activity of aaNAT2 and aaNAT5b clearly demonstrate that A. aegypti has histamine NAT.…”

Section: Resultsmentioning

confidence: 99%

Evolution of insect arylalkylamine N -acetyltransferases: Structural evidence from the yellow fever mosquito, Aedes aegypti

Han

Robinson

Ding

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

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Arylalkylamine N-acetyltransferase (aaNAT) catalyzes the transacetylation from acetyl-CoA to arylalkylamines. aaNATs are involved in sclerotization and neurotransmitter inactivation in insects. Phyletic distribution analysis confirms three clusters of aaNAT-like sequences in insects: typical insect aaNAT, polyamine NAT-like aaNAT, and mosquito unique putative aaNAT (paaNAT). Here we studied three proteins: aaNAT2, aaNAT5b, and paaNAT7, each from a different cluster. aaNAT2, a protein from the typical insect aaNAT cluster, uses histamine as a substrate as well as the previously identified arylalkylamines. aaNAT5b, a protein from polyamine NAT -like aaNAT cluster, uses hydrazine and histamine as substrates. The crystal structure of aaNAT2 was determined using single-wavelength anomalous dispersion methods, and that of native aaNAT2, aaNAT5b and paaNAT7 was detected using molecular replacement techniques. All three aaNAT structures have a common fold core of GCN5-related N-acetyltransferase superfamily proteins, along with a unique structural feature: helix/helices between β3 and β4 strands. Our data provide a start toward a more comprehensive understanding of the structure-function relationship and physiology of aaNATs from the mosquito Aedes aegypti and serve as a reference for studying the aaNAT family of proteins from other insect species. The structures of three different types of aaNATs may provide targets for designing insecticides for use in mosquito control.biogenic amine | melatonin synthesis | catecholamine | insect cuticle

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Section: Resultsmentioning

confidence: 99%

Evolution of insect arylalkylamine N -acetyltransferases: Structural evidence from the yellow fever mosquito, Aedes aegypti

Han

Robinson

Ding

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

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“…Histamine has been recognized for several years as the major neurotransmitter of arthropod photoreceptors (1,2). In Drosophila, immunocytochemistry has shown high levels of histamine in photoreceptors and their synapses (2,3).…”

Section: From the Merck Research Laboratories Merck And Co Inc Rmentioning

confidence: 99%

“…In Drosophila, immunocytochemistry has shown high levels of histamine in photoreceptors and their synapses (2, 3). Further, histidine decarboxylase activity has been demonstrated in Drosophila photoreceptors, suggesting that histamine is synthesized in these cells (2). Drosophila mutants that are deficient in the hdc gene coding for histamine decarboxylase have been identified (4), and flies homozygous for the null mutation appear to be blind (5).…”

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confidence: 99%

Identification of Two Novel Drosophila melanogaster Histamine-gated Chloride Channel Subunits Expressed in the Eye

Hirschberg

Yuan

et al. 2002

Journal of Biological Chemistry

156

151

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Histamine has been shown to play a role in arthropod vision; it is the major neurotransmitter of arthropod photoreceptors. Histamine-gated chloride channels have been identified in insect optic lobes. We report the first isolation of cDNA clones encoding histamine-gated chloride channel subunits from the fruit fly Drosophila melanogaster. The encoded proteins, HisCl1 and HisCl2, share 60% amino acid identity with each other. The closest structural homologue is the human glycine ␣3 receptor, which shares 45 and 43% amino acid identity respectively. Northern hybridization analysis suggested that hisCl1 and hisCl2 mRNAs are predominantly expressed in the insect eye. Oocytes injected with in vitro transcribed RNA, encoding either HisCl1 or HisCl2, produced substantial chloride currents in response to histamine but not in response to GABA, glycine, and glutamate. The histamine sensitivity was similar to that observed in insect laminar neurons. Histamine-activated currents were not blocked by picrotoxinin, fipronil, strychnine, or the H2 antagonist cimetidine. Co-injection of both hisCl1 and hisCl2 RNAs resulted in expression of a histamine-gated chloride channel with increased sensitivity to histamine, demonstrating coassembly of the subunits. The insecticide ivermectin reversibly activated homomeric HisCl1 channels and, more potently, HisCl1 and HisCl2 heteromeric channels.Histamine has been recognized for several years as the major neurotransmitter of arthropod photoreceptors (1, 2). In Drosophila, immunocytochemistry has shown high levels of histamine in photoreceptors and their synapses (2, 3). Further, histidine decarboxylase activity has been demonstrated in Drosophila photoreceptors, suggesting that histamine is synthesized in these cells (2). Drosophila mutants that are deficient in the hdc gene coding for histamine decarboxylase have been identified (4), and flies homozygous for the null mutation appear to be blind (5). Although light-dependent release of histamine from photoreceptors has not yet been demonstrated, exposure of the fly postsynaptic neuron to histamine mimics the effects of light (6).Phototransduction of invertebrates has been most extensively studied in insects, but histamine has been implicated as a neurotransmitter in photoreceptors of several other invertebrate species including barnacles and the horseshoe crab Limulus (7,8), whereas glycine and GABA 1 function as the inhibitory neurotransmitters in vertebrate phototransduction (9). Outside of phototransduction, histamine also appears to be the neurotransmitter in some mechanosensory neurons in Drosophila (10) and in lobster stomatogastric, cardiac, and olfactory neurons (11-13). To date, the molecular nature of the histamine receptor in these neurons is unknown. The laminar neurons that are postsynaptic to insect photoreceptors respond to light with a rapid, chloride-mediated hyperpolarization that can be mimicked by application of histamine (6). These laminar neurons were isolated from optic lobes of several insect species, and the hista...

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“…It is worth noting that, in the mammalian CNS, synapse maintenance, rather than synapse formation, depends on synaptic transmission (62). The early effect on axon behavior we have observed by eliminating acetylcholine, on the other hand, is clearly distinct from the role acetylcholine assumes at the synapse, a point underscored by the fact that acetylcholine is not synthesized by mature photoreceptors, which use histamine as the transmitter for phototransduction (8,9). Our data present clear evidence for an early and somewhat unconventional role of acetylcholine in vivo in the initial formation of projection pattern of photoreceptor axons.…”

Section: Discussionmentioning

confidence: 82%

“…In this system, light transduction depends on synthesis and delivery of the transmitter histamine by the photoreceptor neurons of the retina (8,9). We show that transient developmental synthesis and local secretion of acetylcholine by photoreceptor axons is required for normal growth cone behavior.…”

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confidence: 99%

Nonvesicular release of acetylcholine is required for axon targeting in theDrosophilavisual system

Yang

Kunes²

2004

Proc. Natl. Acad. Sci. U.S.A.

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We report evidence for a developmental role of acetylcholine in axon pathfinding in the Drosophila visual system. Acetylcholine was detected on photoreceptor axons during their navigation to target sites in the brain, a time well before the formation of functional synapses. The pattern of photoreceptor axon projections was severely disrupted when acetylcholine synthesis or metabolism was altered or eliminated, or when transgenic ␣-bungarotoxin, a nicotinic acetylcholine receptor antagonist, was expressed in the developing eye or brain. The requirement for acetylcholine signaling exists before photoreceptor neurons form synaptic connections and does not require the function of vesicular acetylcholine transporter protein. That this early effect of acetylcholine is mediated through nonvesicular release is further supported by the observation that transgenic expression of tetanus toxin, a blocker of neurotransmitter release via synaptic vesicles, did not cause similar photoreceptor axon projection defects. These observations support the notion that a form of acetylcholine secretion mediates the behavior of growth cones during axon pathfinding.I t has been generally thought that the release of neurotransmitter at axon terminals reflects synaptic activity and contributes to the development of synaptic connectivity via activitydependent processes. However, a growing body of evidence suggests that neurotransmitters function in early development in processes that can be independent of synapses or synaptic activity, such as cell proliferation, differentiation, migration, axon outgrowth, and axon branching. In these roles, neurotransmitters are apparently released by mechanisms that are distinct from the conventional synaptic vesicular pathway (1, 2). For example, it has been shown that the neurotransmitters ␥-aminobutyric acid and glutamate can be released in a Ca 2ϩ -and soluble N-ethylmaleimide-sensitive factor attachment protein receptor-independent manner, before synapse formation (3).The effects of loss of acetylcholine synthesis on branching patterns of motor axons is particularly interesting in light of the earlier observation that neurotransmitters may function as chemical signals in axon pathfinding. Experiments on isolated embryonic chick and Xenopus neurons (4, 5) and Drosophila CNS neurons (6) have indicated that the transmitter acetylcholine is synthesized very early in neural development and is present on growing axons well before they reach their target fields or establish functional synapses. Experiments in culture have supported the notion that acetylcholine may have a role in axon navigation. An acetylcholine gradient can cause a growth cone to change direction (7). These studies raise the possibility that nonsynaptic release of neurotransmitter might play a role in regulating growth cone behavior before synaptogenesis.We have undertaken an investigation of the role of small molecule neurotransmitters in the development of the Drosophila visual system. In this system, light transduction depends on synthe...

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Histamine: A Neurotransmitter Candidate for Drosophila Photoreceptors

Cited by 90 publications

References 59 publications

Evolution of insect arylalkylamine N -acetyltransferases: Structural evidence from the yellow fever mosquito, Aedes aegypti

Evolution of insect arylalkylamine N -acetyltransferases: Structural evidence from the yellow fever mosquito, Aedes aegypti

Identification of Two Novel Drosophila melanogaster Histamine-gated Chloride Channel Subunits Expressed in the Eye

Nonvesicular release of acetylcholine is required for axon targeting in theDrosophilavisual system

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